Shape, size, and maturity trajectories of the human ilium.

Morphological traits of the ilium have consistently been more successful for juvenile sex determination than have techniques applied to other skeletal elements, however relatively little is known about the ontogeny and maturation of size and shape dimorphism in the ilium. We use a geometric morphometric approach to quantitatively separate the ontogeny of size and shape of the ilium, and analyze interpopulation differences in the onset, rate and patterning of sexual dimorphism. We captured the shape of three traits for a total of 191 ilia from Lisbon (Portugal) and London (UK) samples of known age and sex (0-17 years). Our results indicate that a) there is a clear dissociation between the ontogeny of size and shape in males and females, b) the ontogeny of size and shape are each defined by non-linear trajectories that differ between the sexes, c) there are interpopulation differences in ontogenetic shape trajectories, which point to population-specific patterning in the attainment of sexual dimorphism, and d) the rate of shape maturation and size maturation is typically higher for females than males. Male and female shape differences in the ilium are brought about by trajectory divergence. Differences in size and shape maturation between the sexes suggest that maturity may confound our ability to discriminate between the sexes by introducing variation not accounted for in age-based groupings. The accuracy of sex determination methods using the ilium may be improved by the use of different traits for particular age groups, to capture the ontogenetic development of shape in both sexes.

[1]  H. Cardoso Environmental effects on skeletal versus dental development: Using a documented subadult skeletal sample to test a basic assumption in human osteological research. , 2007, American journal of physical anthropology.

[2]  B. Shea Ontogenetic approaches to sexual dimorphism in anthropoids , 1986 .

[3]  A. Rosas,et al.  Craniofacial levels and the morphological maturation of the human skull , 2006, Journal of anatomy.

[4]  A. Malgosa,et al.  Ilium growth study: applicability in sex and age diagnosis. , 2005, Forensic science international.

[5]  M. Schillaci,et al.  Brief communication: Sexual dimorphism of the juvenile basicranium. , 2009, American journal of physical anthropology.

[6]  Antonio Rosas,et al.  Thin-plate spline analysis of allometry and sexual dimorphism in the human craniofacial complex. , 2002, American journal of physical anthropology.

[7]  L. Aiello,et al.  Ontogeny of facial dimorphism and patterns of individual development within one human population. , 2006, American journal of physical anthropology.

[8]  R. Tague Variation in pelvic size between males and females. , 1989, American journal of physical anthropology.

[9]  R. Sutter Nonmetric subadult skeletal sexing traits: I. A blind test of the accuracy of eight previously proposed methods using prehistoric known-sex mummies from northern Chile. , 2003, Journal of forensic sciences.

[10]  C. Soligo,et al.  Allometric shape vector projection: a new method for the identification of allometric shape characters and trajectories applied to the human astragalus (talus). , 2011, Journal of theoretical biology.

[11]  F. Williams,et al.  Ontogeny and Phylogeny of the Pelvis in Gorilla, Pongo, Pan, Australopithecus and Homo , 2007, Folia Primatologica.

[12]  Marta Mirazón Lahr,et al.  The problem of assessing landmark error in geometric morphometrics: theory, methods, and modifications. , 2007, American journal of physical anthropology.

[13]  L. Konigsberg,et al.  Statistical study of sexual dimorphism in the human fetal sciatic notch. , 1995, American journal of physical anthropology.

[14]  P. Velemínský,et al.  Technical note: geometric morphometrics and sexual dimorphism of the greater sciatic notch in adults from two skeletal collections: the accuracy and reliability of sex classification. , 2013, American journal of physical anthropology.

[15]  K. Mardia,et al.  Statistical Shape Analysis , 1998 .

[16]  H. Cardoso,et al.  On the reliability of a geometric morphometric approach to sex determination: a blind test of six criteria of the juvenile ilium. , 2011, Forensic science international.

[17]  G. Arnqvist,et al.  Measurement error in geometric morphometrics : Empirical strategies to assess and reduce its impact on measures of shape , 1998 .

[18]  M. Grumbach,et al.  The Neuroendocrinology of Human Puberty Revisited , 2004, Hormone Research in Paediatrics.

[19]  Phillip L Walker,et al.  Greater sciatic notch morphology: sex, age, and population differences. , 2005, American journal of physical anthropology.

[20]  H. Cardoso,et al.  Environmental effects on skeletal versus dental development II: further testing of a basic assumption in human osteological research. , 2011, American journal of physical anthropology.

[21]  P. O'higgins,et al.  A geometric morphometric study of regional differences in the ontogeny of the modern human facial skeleton † , 2002, Journal of anatomy.

[22]  E. Crelin SECTION OF BIOLOGICAL AND MEDICAL SCIENCES: THE DEVELOPMENT OF THE BONY PELVIS AND ITS CHANGES DURING PREGNANCY AND PARTURITION* , 1969 .

[23]  F. Bookstein,et al.  Heterochrony and geometric morphometrics: a comparison of cranial growth in Pan paniscus versus Pan troglodytes , 2005, Evolution & development.

[24]  M. Roksandic,et al.  Greater sciatic notch as a sex indicator in juveniles. , 2008, American journal of physical anthropology.

[25]  W. Cleveland Robust Locally Weighted Regression and Smoothing Scatterplots , 1979 .

[26]  R. Tibshirani,et al.  An introduction to the bootstrap , 1993 .

[27]  L. F. Marcus,et al.  Advances in Morphometrics , 1996, NATO ASI Series.

[28]  P. O'higgins,et al.  Sexual Dimorphism in the Subadult Mandible: Quantification Using Geometric Morphometrics * , 2007, Journal of forensic sciences.

[29]  J. Plavcan,et al.  Taxonomic variation in the patterns of craniofacial dimorphism in primates. , 2002, Journal of human evolution.

[30]  William G. Jacoby Loess: a nonparametric, graphical tool for depicting relationships between variables , 2000 .

[31]  P. O'higgins,et al.  Sexual dimorphism and facial growth in papionin monkeys , 2002 .

[32]  E. Crelin,et al.  THE DEVELOPMENT OF BONY PELVIC SEXUAL DIMORPHISM IN MICE * , 1960 .

[33]  P. O’Higgins,et al.  The ontogeny of sexual dimorphism in the facial skeleton of the African apes. , 2007, Journal of human evolution.

[34]  Trish E. Parsons,et al.  Deciphering the Palimpsest: Studying the Relationship Between Morphological Integration and Phenotypic Covariation , 2009, Evolutionary Biology.

[35]  D. Mittler,et al.  Sex determination in subadults using auricular surface morphology: a forensic science perspective. , 1992, Journal of forensic sciences.

[36]  H. Coqueugniot,et al.  L'utilisation de caractères morphologiques dans la diagnose sexuelle des mandibules d'enfants : application à la collection ostéologique de Turin (Italie) , 2002 .

[37]  H. Cardoso Sample-specific (universal) metric approaches for determining the sex of immature human skeletal remains using permanent tooth dimensions , 2008 .

[38]  E. Crelin,et al.  Bony pelvic sexual dimorphism in the rat , 1967 .

[39]  A. Kuijpers-Jagtman,et al.  Geometric morphometric analysis of craniofacial variation, ontogeny and modularity in a cross‐sectional sample of modern humans , 2013, Journal of anatomy.

[40]  T W Phenice,et al.  A newly developed visual method of sexing the os pubis. , 1969, American journal of physical anthropology.

[41]  M. Lavelle,et al.  Natural selection and developmental sexual variation in the human pelvis. , 1995, American journal of physical anthropology.

[42]  C. Goodall Procrustes methods in the statistical analysis of shape , 1991 .

[43]  Jaroslav Bruzek,et al.  A method for visual determination of sex, using the human hip bone. , 2002, American journal of physical anthropology.

[44]  W. H. Coleman,et al.  Sex differences in the growth of the human bony pelvis. , 1969, American journal of physical anthropology.

[45]  R. Tague Variation in pelvic size between males and females in nonhuman anthropoids. , 1995, American journal of physical anthropology.

[46]  E. Wagenmakers,et al.  AIC model selection using Akaike weights , 2004, Psychonomic bulletin & review.

[47]  S. Mays,et al.  Some Sexually Dimorphic Features of the Human Juvenile Skull and their Value in Sex Determination in Immature Skeletal Remains , 1998 .

[48]  H. Cardoso Brief communication: the collection of identified human skeletons housed at the Bocage Museum (National Museum of Natural History), Lisbon, Portugal. , 2006, American journal of physical anthropology.

[49]  S. Mays,et al.  The effects of socioeconomic status on endochondral and appositional bone growth, and acquisition of cortical bone in children from 19th century Birmingham, England. , 2009, American journal of physical anthropology.

[50]  D. Hunt Sex determination in the subadult ilia: an indirect test of Weaver's nonmetric sexing method. , 1990, Journal of forensic sciences.

[51]  L. Humphrey,et al.  Growth patterns in the modern human skeleton. , 1998, American journal of physical anthropology.

[52]  M. Zelditch,et al.  Studying ontogenetic trajectories using resampling methods and landmark data , 2013 .

[53]  Hervé Rousseau,et al.  Ontogeny of Size and Shape Sexual Dimorphism in the Ilium: A Multislice Computed Tomography Study by Geometric Morphometry , 2013, Journal of forensic sciences.

[54]  N. Macleod,et al.  Morphometric Criteria for Sexing Juvenile Human Skeletons Using the Ilium , 2008, Journal of forensic sciences.

[55]  V. Bernal,et al.  Differences between sliding semi‐landmark methods in geometric morphometrics, with an application to human craniofacial and dental variation , 2006, Journal of anatomy.

[56]  B. Boucher Sex differences in the foetal pelvis. , 1957, American journal of physical anthropology.

[57]  Christian Peter Klingenberg,et al.  Evolution and development of shape: integrating quantitative approaches , 2010, Nature Reviews Genetics.

[58]  H. Rousseau,et al.  Sexual Dimorphism of the Fetal Ilium: A 3D Geometric Morphometric Approach with Multislice Computed Tomography , 2013, Journal of forensic sciences.

[59]  C. Farquharson,et al.  The role of sex steroids in controlling pubertal growth , 2008, Clinical endocrinology.

[60]  M Steyn,et al.  Sexually dimorphic pelvic morphology in South African whites and blacks. , 2003, Homo : internationale Zeitschrift fur die vergleichende Forschung am Menschen.

[61]  P. O'higgins,et al.  Facial growth and the ontogeny of morphological variation within and between the primates Cebus apella and Cercocebus torquatus , 2001 .

[62]  V. Bernal,et al.  Ontogeny of robusticity of craniofacial traits in modern humans: a study of South American populations. , 2009, American journal of physical anthropology.

[63]  H. Akaike A new look at the statistical model identification , 1974 .

[64]  S. Saunders,et al.  Two arch criteria of the ilium for sex determination of immature skeletal remains: a test of their accuracy and an assessment of intra- and inter-observer error. , 2008, Forensic science international.

[65]  Jesús Marugán-Lobón,et al.  Evolutionary covariation in geometric morphometric data: analyzing integration, modularity, and allometry in a phylogenetic context. , 2013, Systematic biology.

[66]  M. Henneberg,et al.  Sexually dimorphic mandibular morphology in the first few years of life. , 2001, American journal of physical anthropology.

[67]  M. Zelditch,et al.  The ontogenetic dynamics of shape disparity , 2003, Paleobiology.

[68]  Peter Dangerfield,et al.  Developmental Juvenile Osteology. By LOUISE SCHEUER and SUE BLACK. (Pp. x+587; fully illustrated; $159 hardback; ISBN 0 12 624000 0.) San Diego: Academic Press. 2000 , 2001 .

[69]  N. Chattopadhyay,et al.  The role of estrogen in bone growth and formation: changes at puberty , 2010 .

[70]  M. Zelditch,et al.  The complex ontogenetic trajectory of mandibular shape in a laboratory mouse , 2013, Journal of anatomy.

[71]  G. Karsenty,et al.  CHAPTER 4 – Postnatal Bone Growth: Growth Plate Biology, Modeling, and Remodeling , 2003 .

[72]  D. Weaver,et al.  Sex differences in the ilia of a known sex and age sample of fetal and infant skeletons. , 1980, American journal of physical anthropology.

[73]  L. A. Wilson The contribution of developmental palaeontology to extensions of evolutionary theory , 2013 .

[74]  D. J. Millward,et al.  Catch-up growth in children. , 2009, Nutrition reviews.

[75]  Louise Scheuer,et al.  A blind test of mandibular morphology for sexing mandibles in the first few years of life. , 2002, American journal of physical anthropology.

[76]  A. Rosas,et al.  Facial heights: evolutionary relevance of postnatal ontogeny for facial orientation and skull morphology in humans and chimpanzees. , 2004, Journal of human evolution.

[77]  S. Washburn Sex differences in the pubic bone. , 1948, American journal of physical anthropology.

[78]  F. Rohlf,et al.  Extensions of the Procrustes Method for the Optimal Superimposition of Landmarks , 1990 .

[79]  Fred L. Bookstein,et al.  Landmark methods for forms without landmarks: morphometrics of group differences in outline shape , 1997, Medical Image Anal..

[80]  M. Foote Contributions of individual taxa to overall morphological disparity , 1993, Paleobiology.

[81]  H. Schutkowski,et al.  Sex determination of infant and juvenile skeletons: I. Morphognostic features. , 1993, American journal of physical anthropology.

[82]  Theodore Garland,et al.  Developmental regulation of skull morphology II: ontogenetic dynamics of covariance , 2004, Evolution & development.